Sex differences in amygdala subregions: evidence from subregional shape analysis
Abstract
Each subregion of the amygdala is characterized by a distinct cytoarchitecture and function. However, most previous studies on sexual dimorphism and aging have assessed differences in the structure of the amygdala at the level of the amygdala in its entirety rather than at the subregional level. Using an amygdala subregional shape analysis, we investigated the effects of sex, age, and the sex × age interaction on the subregion after controlling for intracranial volume. We found the main effect of age in the subregions and the effect of sex in the superficial nucleus, which showed that men had a larger mean radius than women. We also found a sex × age interaction in the centromedial nucleus, in that the radius of the centromedial nucleus showed a steeper decline with age in women compared with men. Regarding the amygdala volume as a whole, we found only an age effect and did not find any other significant difference between genders. The sex difference in the amygdala subregion and its relevance to the circulating gonadal hormone were discussed.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Prior studies in adults have found sex differences in the shape and volume of amygdala sub-regions and in resting-state functional connectivity of non-limbic brain regions.
“Previous studies in adults have reported sex differences in amygdala sub-region shape and volume (Kim et al., 2011, Kim et al., 2012) and in RSFC of non-limbic brain regions using a variety of analytic methods (Kilpatrick et al., 2006, Biswal et al., 2010, Tian et al., 2011, Casanova et al., 2012, Satterthwaite et al., 2014).”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Kim et al., 2012
Cites
Intraclass correlations: Uses in assessing rater reliability.
Shrout, P. E., & Fleiss, J. L. (1979) · Psychological Bulletin · doi:10.1037/0033-2909.86.2.420 · Cited by 23,433 · see citing works
Ashburner, J., & Friston, K. J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.02.018 · Cited by 7,507 · see citing works
Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data
Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C., Watkins, K., Ciccarelli, O., Cader, M., Matthews, P., et al. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.02.024 · Cited by 6,035 · see citing works
A nonparametric method for automatic correction of intensity nonuniformity in MRI data
Sled, J. G., Zijdenbos, A. P., & Evans, A. C. (1998) · IEEE Transactions on Medical Imaging · doi:10.1109/42.668698 · Cited by 4,731 · see citing works
A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains
Good, C. D., Johnsrude, I. S., Ashburner, J., Henson, R. N. A., Friston, K. J., & Frackowiak, R. S. J. (2001) · NeuroImage · doi:10.1006/nimg.2001.0786 · Cited by 4,561 · see citing works
A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data
Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., & Zilles, K. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.12.034 · Cited by 4,033 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.2.274 · Cited by 3,262 · see citing works
Bayesian analysis of neuroimaging data in FSL
Woolrich, M., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T. E. J., Beckmann, C., Jenkinson, M., & Smith, S. M. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.10.055 · Cited by 2,774 · see citing works
Simerly, R. B., Swanson, L. W., Chang, C., & Muramatsu, M. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.902940107 · Cited by 2,118 · see citing works
Why sex matters for neuroscience
Cahill, L. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1909 · Cited by 1,540 · see citing works
Pfefferbaum, A., Mathalon, D. H., Sullivan, E. V., Rawles, J. M., Zipursky, R. B., & Lim, K. O. (1994) · Archives of Neurology · doi:10.1001/archneur.1994.00540210046012 · Cited by 1,363 · see citing works
Swanson, L. W., & Petrovich, G. D. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01265-x · Cited by 1,351 · see citing works
Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., Habel, U., Schneider, F., & Zilles, K. (2005) · Anatomy and Embryology · doi:10.1007/s00429-005-0025-5 · Cited by 1,264 · see citing works
Raz, N. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.3.268 · Cited by 1,239 · see citing works
Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease
Jack, C. R., Petersen, R. C., Xu, Y. C., Waring, S. C., O'Brien, P. C., Tangalos, E. G., Smith, G. E., Ivnik, R. J., & Kokmen, E. (1997) · Neurology · doi:10.1212/wnl.49.3.786 · Cited by 1,128 · see citing works
Normal Sexual Dimorphism of the Adult Human Brain Assessed by In Vivo Magnetic Resonance Imaging
Goldstein, J. M. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.6.490 · Cited by 1,021 · see citing works
The Amygdala: a functional analysis
Aggleton, J. P. (2000) · Cited by 964 · see citing works
Functional connectivity of the human amygdala using resting state fMRI
Roy, A. K., Shehzad, Z., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Gotimer, K., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.11.030 · Cited by 749 · see citing works
Pruessner, J. C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.4.433 · Cited by 706 · see citing works
One-Year Brain Atrophy Evident in Healthy Aging
Fjell, A. M., Walhovd, K. B., Fennema-Notestine, C., McEvoy, L. K., Hagler, D. J., Holland, D., Brewer, J. B., & Dale, A. M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3252-09.2009 · Cited by 692 · see citing works
Jorm, A. F. (2000) · Psychological Medicine · doi:10.1017/s0033291799001452 · Cited by 655 · see citing works
Effects of age on volumes of cortex, white matter and subcortical structures
Walhovd, K. B., Fjell, A. M., Reinvang, I., Lundervold, A., Dale, A. M., Eilertsen, D. E., Quinn, B. T., Salat, D. H., Makris, N., & Fischl, B. R. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.05.020 · Cited by 647 · see citing works
Men and women differ in amygdala response to visual sexual stimuli
Hamann, S., Herman, R. A., Nolan, C. L., & Wallen, K. (2004) · Nature Neuroscience · doi:10.1038/nn1208 · Cited by 603 · see citing works
Morey, R. A., Petty, C. M., Xu, Y., Pannu Hayes, J., Wagner, H. R., Lewis, D. V., LaBar, K. S., Styner, M., & McCarthy, G. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.12.033 · Cited by 540 · see citing works
One-year Age Changes in MRI Brain Volumes in Older Adults
Resnick, S. M. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.5.464 · Cited by 517 · see citing works
Hippocampal morphometry in schizophrenia by high dimensional brain mapping
Csernansky, J. G., Joshi, S. C., Wang, L., Haller, J. W., Gado, M. H., Miller, J. P., Grenander, U., & Miller, M. I. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.19.11406 · Cited by 469 · see citing works
Gender differences in age effect on brain atrophy measured by magnetic resonance imaging.
Gur, R., Mozley, P., Resnick, S., Gottlieb, G., Kohn, M., Zimmerman, R. A., Herman, G., Atlas, S. J., Grossman, R., & Berretta, D. (1991) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.88.7.2845 · Cited by 467 · see citing works
The Role of the Central Nucleus of the Amygdala in Mediating Fear and Anxiety in the Primate
Kalin, N. H., Shelton, S. E., & Davidson, R. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0292-04.2004 · Cited by 406 · see citing works
Sex Differences in Temporo-limbic and Frontal Brain Volumes of Healthy Adults
Gur, R. C. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.9.998 · Cited by 403 · see citing works
Österlund, M. K., Kuiper, G. G. J. M., Gustafsson, J.-Α., & Hurd, Y. L. (1998) · Molecular Brain Research · doi:10.1016/s0169-328x(97)00351-3 · Cited by 378 · see citing works
Hormonal Cycle Modulates Arousal Circuitry in Women Using Functional Magnetic Resonance Imaging
Goldstein, J. M., Jerram, M., Poldrack, R., Ahern, T., Kennedy, D. N., Seidman, L. J., & Makris, N. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2239-05.2005 · Cited by 368 · see citing works
Hippocampus and Amygdala Morphology in Attention-Deficit/Hyperactivity Disorder
Plessen, K. J., Bansal, R., Zhu, H., Whiteman, R., Amat, J., Quackenbush, G. A., Martin, L., Durkin, K., Blair, C., Royal, J., et al. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.7.795 · Cited by 347 · cited 2× · see citing works
“In this regard, methods for assessing the shape contour of the amygdala were developed and successfully applied to detect small changes in the amygdalae of patients with psychiatric or neurological diseases (Chung et al., 2010; Kim et al., 2010; Peterson et al., 2007; Plessen et al., 2006; Qiu et al., 2009; Shenton et…”
Hermans, E. J., Ramsey, N. F., & van Honk, J. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.05.013 · Cited by 339 · see citing works
Sex differences in aging of the human frontal and temporal lobes
Cowell, P. E., Turetsky, B. I., Gur, R., Grossman, R. I., Shtasel, D. L., & Gur, R. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-08-04748.1994 · Cited by 336 · see citing works
A brain sexual dimorphism controlled by adult circulating androgens
Cooke, B. M., Tabibnia, G., & Breedlove, S. M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.13.7538 · Cited by 311 · see citing works
Sex chromosome genes directly affect brain sexual differentiation
Carruth, L. L., Reisert, I., & Arnold, A. P. (2002) · Nature Neuroscience · doi:10.1038/nn922 · Cited by 298 · see citing works
Wrase, J., Vollstädt‐Klein, S., Gruesser, S. M., Hermann, D., Flor, H., Mann, K. F., Braus, D. F., & Heinz, A. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00565-2 · Cited by 284 · see citing works
Localization of Deformations Within the Amygdala in Individuals With Psychopathy
Yang, Y., Raine, A., Narr, K. L., Colletti, P. M., & Toga, A. W. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.110 · Cited by 284 · see citing works
Österlund, M. K., Gustafsson, J.-Α., Keller, É., & Hurd, Y. L. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.10.6913 · Cited by 273 · see citing works
Ageing of the Hypothalamo-Pituitary- Testicular Axis in Men
Vermeulen, A., & Kaufman, J. M. (2008) · Hormone Research · doi:10.1159/000184233 · Cited by 265 · cited 2× · see citing works
“In addition, because the slope of age-related changes in the level of gonadal hormones differs between men and women (Bjørnerem et al., 2004; Vermeulen and Kaufman, 1995), variances in both the type and amount of sex steroids may also contribute to gender-specific aging patterns in the morphology of the CM.”
Age-related decline in MRI volumes of temporal lobe gray matter but not hippocampus
Sullivan, E. V., Marsh, L., Mathalon, D. H., Lim, K. O., & Adolf Pfefferbaum, A. (1995) · Neurobiology of Aging · doi:10.1016/0197-4580(95)00074-o · Cited by 256 · see citing works
A call to action: overcoming anxiety through active coping.
LeDoux, J. E., & Gorman, J. M. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.12.1953 · Cited by 238 · see citing works
Ebner, K., Rupniak, N. M. J., Saria, A., & Singewald, N. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400794101 · Cited by 225 · see citing works
Symptoms of depression and anxiety during adult life: evidence for a decline in prevalence with age
Henderson, A. S., Jorm, A. F., Korten, A. E., Jacomb, P. A., Christensen, H. M., & Rodgers, B. (1998) · Psychological Medicine · doi:10.1017/s0033291798007570 · Cited by 208 · see citing works
Bjørnerem, Å., Straume, B., Midtby, M., Fønnebø, V., Sundsfjord, J., Svartberg, J., Acharya, G., Øian, P., & Berntsen, G. K. R. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-0735 · Cited by 199 · see citing works
Mu, Q., Xie, J., Wen, Z., Weng, Y., & Shuyun, Z. (1999) · PubMed Central · Cited by 189 · see citing works
Lehman, M. N., & Winans, S. S. (1982) · Brain Research · doi:10.1016/0006-8993(82)90641-2 · Cited by 188 · see citing works
Sexual difference in nuclear volume and its ontogeny in the rat amygdala
Mizukami, S., Nishizuka, M., & Arai, Y. (1983) · Experimental Neurology · doi:10.1016/0014-4886(83)90235-2 · Cited by 178 · see citing works
Ball, T., Rahm, B., Eickhoff, S. B., Schulze-Bonhage, A., Speck, O., & Mutschler, I. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000307 · Cited by 176 · see citing works
General multivariate linear modeling of surface shapes using SurfStat
Chung, M. K., Worsley, K. J., Nacewicz, B. M., Dalton, K. M., & Davidson, R. J. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.06.032 · Cited by 159 · see citing works
Regional shape abnormalities in mild cognitive impairment and Alzheimer's disease
Qiu, A., Fennema‐Notestine, C., Dale, A. M., & Miller, M. I. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.01.013 · Cited by 155 · see citing works
Sex Differences in the Vomeronasal System
Guillamón, A., & Segovia, S. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00217-7 · Cited by 150 · see citing works
Testosterone Increases Amygdala Reactivity in Middle-Aged Women to a Young Adulthood Level
van Wingen, G. A., Zylicz, S. A., Pieters, S., Mattern, C., Verkes, R. J., Buitelaar, J. K., & Fernández, G. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.2 · Cited by 144 · see citing works
Morphologic Features of the Amygdala and Hippocampus in Children and Adults With Tourette Syndrome
Peterson, B. S., Choi, H. A., Hao, X., Amat, J., Hongtu Zhu, B., Whiteman, R. C., Liu, J., Xu, D., & Bansal, R. (2007) · Archives of General Psychiatry · doi:10.1001/archpsyc.64.11.1281 · Cited by 139 · see citing works
Meisami, E., MIKHAIL, L., BAIM, D., & Bhatnagar, K. P. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb10649.x · Cited by 137 · see citing works
Shenton, M. E., Gerig, G., McCarley, R. W., Székely, G. J., & Kikinis, R. (2002) · Psychiatry Research Neuroimaging · doi:10.1016/s0925-4927(02)00025-2 · Cited by 137 · see citing works
Gizewski, E. R., Krause, E., Karama, S., Baars, A., Senf, W., & Forsting, M. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0429-3 · Cited by 133 · see citing works
Fjell, A. M., Westlye, L. T., Amlien, I. K., Espeseth, T., Reinvang, I., Raz, N., Agartz, I., Salat, D. H., Greve, D. N., Fischl, B. R., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0115-09.2009 · Cited by 125 · see citing works
Morris, J. A., Jordan, C. L., & Breedlove, S. M. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21536 · Cited by 109 · see citing works
Laterobasal Amygdalar Enlargement in 6- to 7-Year-Old Children With Autism Spectrum Disorder
Kim, J. E., Lyoo, I. K., Estes, A. M., Renshaw, P. F., Shaw, D., Friedman, S. D., Kim, D. J., Yoon, S. J., Hwang, J., & Dager, S. R. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.148 · Cited by 95 · see citing works
Roselli, C. E., Klosterman, S., & Resko, J. A. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1343 · Cited by 91 · see citing works
Gonzalez-Lima, F., & Scheich, H. (1986) · Brain Research · doi:10.1016/0006-8993(86)91009-7 · Cited by 76 · see citing works
Bloom, F. E., Björklund, A., & Hökfelt, T. G. M. (1997) · Elsevier eBooks · Cited by 75 · see citing works
Automatic and Robust Computation of 3D Medial Models Incorporating Object Variability
Styner, M. A., Gerig, G., Joshi, S. C., et al. (2003) · International Journal of Computer Vision · doi:10.1023/a:1026378916288 · Cited by 75 · see citing works
Functional activation of the left amygdala and hippocampus during associative encoding
Killgore, W. D. S., Casasanto, D., Yurgelun-Todd, D., Maldjian, J., & Detre, J. (2000) · NeuroReport · doi:10.1097/00001756-200007140-00039 · Cited by 63 · see citing works
Amygdalae morphometry in late-life depression
Tamburo, R., Siegle, G., Stetten, G., Cois, C. A., Butters, M., Reynolds, C., & Aizenstein, H. (2009) · International Journal of Geriatric Psychiatry · doi:10.1002/gps.2167 · Cited by 40 · see citing works
Sex differences in the posteromedial cortical nucleus of the amygdala in the rat
Vinader‐Caerols, C., Collado, P., Segovia, S., & Guillamón, A. (1998) · Neuroreport · doi:10.1097/00001756-199808030-00042 · Cited by 35 · see citing works
Kim, N., Kim, H. J., Hwang, J., Yoon, S. J., Cho, H. B., Renshaw, P. F., Lyoo, I. K., & Kim, J. E. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2010.11.005 · Cited by 11 · see citing works
Self-citationThe Primate Nervous System, Part III
(1999) · Handbook of chemical neuroanatomy · doi:10.1016/s0924-8196(99)x8001-8 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Developmental sex differences in resting state functional connectivity of amygdala sub-regions
Alarcón, G., Cservenka, A., Rudolph, M. D., Fair, D. A., & Nagel, B. J. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.04.013 · Cited by 105 · see citing works
- Authors
- Kim, H. J., Kim, N., Kim, S., Hong, S., Park, K., Lim, S., Park, J.-M., Na, B., Chae, Y., Lee, J., Yeo, S., Choe, I.-H., Cho, S.-Y., & Cho, G.
- Affiliations
- Korea Basic Science Institute (KR)
- Asan Medical Center (KR)
- Kyung Hee University (KR)
- Seoul National University (KR)
- Corresponding author
- Cho, Gyunggoo
- ORCID
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2012-05
- Volume
- 60
- Issue
- 4
- Pages
- 2054-2061
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W1975261610
- Cited by
- 40
- References
- 70
- Citations by year
- 2026: 3 · 2024: 2 · 2023: 2 · 2022: 2 · 2021: 3 · 2020: 2 · 2019: 2 · 2018: 3 · 2016: 6 · 2015: 3 · 2014: 3 · 2013: 6 · 2012: 3
- FWCI
- 2.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Korea Basic Science Institute (T30403)
- National Research Foundation of Korea
- Ministry of Education, Science and Technology (0023051)
- Ministry of Education and Human Resources Development (KRF-2007-511-H00002)
- Ministry of Health and Welfare (A090754)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Sex and Gender in Healthcare
- Keywords
- amygdala, sex differences, sexual dimorphism, amygdala subregions, aging, gonadal hormones, brain structure
- MeSH terms
- Adult, Aged, Amygdala, Female, Humans, Image Interpretation, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Sex Characteristics, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review